The PapG tip adhesin of P fimbriae protects Escherichia coli from neutrophil bactericidal activity

Abstract

Compared with Escherichia coli ORN103, a nonfimbriated K-12 strain, P-fimbriated E. coli ORN103/pPAP5 was found to interact poorly with human neutrophils and resist their bactericidal activity in vitro. PapG, the Gal alpha(1-->4)Gal binding moiety located at the distal end of the P fimbrial filament, appeared to be responsible for this effect because an isogenic PapG- mutant, E. coli ORN103/pPAP24, exhibited binding interactions with neutrophils that were similar to nonfimbriated E. coli ORN103. Although no direct evidence is available, the poor adherence mediated by PapG could be related to its electrostatic properties because the isolated PapG protein had a pI of 5.2, which indicated that in the physiological pH range it possessed a net negative charge. Antibodies against PapG overcame the protective effect of PapG and markedly enhanced the interactions of P-fimbriated E. coli with neutrophils resulting in bacterial killing. When a P-fimbriated clinical E. coli strain or its isogenic PapG- derivative was injected into the peritoneal cavities of mice, a similar number of neutrophils was recruited to the site of injection. After 2 h, the number of P-fimbriated E. coli organisms that survived the neutrophil influx in the mouse peritoneum was approximately four times more than the number of surviving PapG- bacteria. This result demonstrates that the PapG protein, which is strategically located at the distal region of the P-fibrillum structure, protects E. coli from the bactericidal action of neutrophils.

TLR‐ and CXCR1‐dependent innate immunity: insights into the genetics of urinary tract infections

“…P fimbriae thus appear to prevent other bacterial surface components from triggering a neutrophil response. In contrast, type 1 fimbriae, which bind mannosylated glycoproteins, activate the oxidative burst [31].…”

Epidemiological Study of pap Genes among Diarrheagenic or Septicemic Escherichia coli Strains Producing CS31A and F17 Adhesins and Characterization of Pap 31A Fimbriae

“…It is well documented that F165 1 fimbriae are required for the full pathogenicity of E. coli strains in gnotobiotic pigs, not for initial colonization of the intestinal mucosa but for systemic bacterial persistence and resistance to phagocytosis (38). Furthermore, among human uropathogenic E. coli strains, P fimbriae are not only responsible for binding to and colonization of the urinary mucosa by E. coli (20) but also protect E. coli strains from the bactericidal activity of human polymorphonuclear neutrophils (40). We speculate that Pap 31A fimbriae could play a role in the resistance to phagocytosis or extraintestinal adherence of E. coli 31A.…”

F1651fimbriae of the P fimbrial family inhibit the oxidative response of porcine neutrophils

“…However, the major structural subunit of these fimbriae appears to inhibit the oxidative response since genetically cloned E. coli strains expressing S‐mannose‐resistant hemagglutination along with S fimbriae (S‐MRH + , S‐Fim + ) could significantly decrease the oxidative response of hPMNs as compared to S‐MRH + , S‐Fim − clones. On the other hand, P fimbriae with binding specificity to Gal‐Gal‐containing receptor inhibit bacterial attachment to and oxidative response of human neutrophils due to a repulsive effect of the PapG adhesin, thus protecting the bacteria from phagocytic killing [13].…”

“…Wild‐type E. coli strain 5131 was isolated from the intestinal contents of a diarrheic and septicemic piglet at the Faculté de Médecine Vétérinaire, Université de Montréal, Saint‐Hyacinthe, Que., Canada. This strain is serum‐resistant, induces septicemia in experimentally inoculated piglets, and is resistant to phagocytic killing by pPMNLs [2–16]. Strain HB101 (pCJ7) is a transformant from plasmid pACYC184 in which was inserted a 10‐kb fragment of DNA (from an F165 1 ‐positive wild‐type septicemia‐inducing E. coli strain 4787) into the Bam HI site [15].…”

“…This interaction results in ingestion of bacteria and stimulation of the phagocyte oxidative response, leading to bacterial killing [11,12]. P fimbriae expressing class I PapG adhesin with specificity for the Gal‐Gal moiety prevent attachment of bacteria to human neutrophils, thus protecting cells from phagocyte bacterial activity [13].…”